Immune insufficiency during GVHD is due to defective antigen presentation within dendritic cell subsets

Blood

Volumn 119, Issue 24, 2012, Pages 5918-5930

  Markey, Kate A ^a   Koyama, Motoko ^a   Kuns, Rachel D ^a   Lineburg, Katie E ^a   Wilson, Yana A ^a   Olver, Stuart D ^a   Raffelt, Neil C ^a   Don, Alistair L J ^a   Varelias, Antiopi ^a   Robb, Renee J ^a,b   Cheong, Melody ^a   Engwerda, Christian R ^a   Steptoe, Raymond J ^b   Ramshaw, Hayley S ^c,d   Lopez, Angel F ^c,d   Vega Ramos, Javier ^e   Lew, Andrew M ^f   Villadangos, Jose A ^e   Hill, Geoffrey R ^a,g   MacDonald, Kelli P A ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c University of Adelaide   (Australia)

^d UNIVERSITY OF ADELAIDE   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^g ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ALLOIMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; GRAFT VERSUS HOST REACTION; IMMUNE DEFICIENCY; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 84862506107     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-12-398164     Document Type: Article

References (50)

1. Hill GR, Crawford JM, Cooke KR, Brinson YS, Pan L, Ferrara JLM. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood. 1997;90(8):3204-3213. (Pubitemid 27444217)
2. Howard JG, Woodruff MFA. Effect of the graft-versus- host reaction on the immunological responsiveness of the mouse. Proc R Soc Lond Biol. 1961;154(957):532-539.
3. Zaleski M, Milgrom F. Immunosuppressive effect of graft-versus-host reaction. Cell Immunol. 1973;7(2):268-274.
4. Elie R, Lapp WS. Graft-versus-host induced immunosuppression: mechanism of depressed T helper cell function in vitro. Cell. Immunol. 1977;34:38.
5. Witherspoon RP, Matthews D, Storb R, et al. Recovery of in vivo cellular immunity after human marrow grafting: influence of time postgrafting and acute graft-versus-host disease. Transplantation. 1984;37(2):145-150. (Pubitemid 14191879)
6. Seddik M, Seemayer TA, Lapp WS. The graft-versus- host reaction and immune function: I. T helper cell immunodeficiency associated with graft-versus-host-induced thymic epithelial cell damage. Transplantation. 1984;37(3):281-286. (Pubitemid 14164943)
7. Paraiso KH, Ghansah T, Costello A, Engelman RW, Kerr WG. Induced SHIP deficiency expands myeloid regulatory cells and abrogates graft-versushost disease. J Immunol. 2007;178(5):2893-2900. (Pubitemid 46333167)
8. Elie R, Lapp WS. Graft versus host-induced immunosuppression: mechanism of depressed T-cell helper function in vitro. Cell Immunol. 1977;34(1):38-48. (Pubitemid 8216165)
9. Capitini CM, Herby S, Milliron M, Anver MR, Mackall CL, Fry TJ. Bone marrow deficient in IFN-γ signaling selectively reverses GVHD-associated immunosuppression and enhances a tumor-specific GVT effect. Blood. 2009;113(20):5002-5009.
10. Dudziak D, Kamphorst AO, Heidkamp GF, et al. Differential antigen processing by dendritic cell subsets in vivo. Science. 2007;315(5808):107-111. (Pubitemid 46196991)
11. Markey KA, Burman AC, Banovic T, et al. Soluble lymphotoxin is an important effector molecule in GVHD and GVL. Blood. 2010;115(1):122-132.
12. Cooke KR, Kobzik L, Martin TR, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 1996;88:3230-3239. (Pubitemid 26357409)
13. Lahl K, Loddenkemper C, Drouin C, et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J Exp Med. 2007;204(1):57-63. (Pubitemid 46148756)
14. MacDonald KP, Kuns RD, Rowe V, et al. Effector and regulatory T-cell function is differentially regulated by RelB within antigen-presenting cells during GVHD. Blood. 2007;109(11):5049-5057. (Pubitemid 46827805)
15. Banovic T, MacDonald KP, Morris ES, et al. TGFbeta in allogeneic stem cell transplantation: friend or foe? Blood. 2005;106(6):2206-2214. (Pubitemid 41291742)
16. Morris ES, MacDonald KP, Rowe V, et al. NKT cell-dependent leukemia eradication following stem cell mobilization with potent G-CSF analogs. J Clin Invest. 2005;115(11):3093-3103. (Pubitemid 41567574)
17. Markey KA, Banovic T, Kuns RD, et al. Conventional dendritic cells are the critical donor APC presenting alloantigen after experimental bone marrow transplantation. Blood. 2009;113(22):5644-5649.
18. Reddy P, Negrin R, Hill GR. Mouse models of bone marrow transplantation. Biol Blood Marrow Transplant. 2008;14(1 suppl 1):129-135. (Pubitemid 350286851)
19. Rudensky A, Rath S, Preston-Hurlburt P, Murphy DB, Janeway CA Jr. On the complexity of self. Nature. 1991;353(6345):660-662. (Pubitemid 21912583)
20. Viret C, Janeway CA Jr. Functional and phenotypic evidence for presentation of E alpha 52-68 structurally related self-peptide(s) in I-E alphadeficient mice. J Immunol. 2000;164(9):4627-4634. (Pubitemid 30238061)
21. Rudensky A, Rath S, Preston-Hurlburt P, Murphy DB, Janeway CA Jr. On the complexity of self. Nature. 1991;353(6345):660-662. (Pubitemid 21912583)
22. Koyama M, Kuns RD, Olver SD, et al. Recipient nonhematopoietic antigen-presenting cells are sufficient to induce lethal acute graft-versus-host disease. Nat Med. 2012;18(1):135-142.
23. Bedoui S, Whitney PG, Waithman J, et al. Crosspresentation of viral and self antigens by skinderived CD103+ dendritic cells. Nat Immunol. 2009;10(5):488-495.
24. Young LJ, Wilson NS, Schnorrer P, et al. Differential MHC class II synthesis and ubiquitination confers distinct antigen-presenting properties on conventional and plasmacytoid dendritic cells. Nat Immunol. 2008;9(11):1244- 1252.
25. Young LJ, Wilson NS, Schnorrer P, et al. Dendritic cell preactivation impairs MHC class II presentation of vaccines and endogenous viral antigens. Proc Natl Acad Sci U S A. 2007;104(45):17753-17758. (Pubitemid 350210907)
26. Schnorrer P, Behrens GM, Wilson NS, et al. The dominant role of CD8+ dendritic cells in crosspresentation is not dictated by antigen capture. Proc Natl Acad Sci U S A. 2006;103(28):10729-10734. (Pubitemid 44078044)
27. Allan RS, Waithman J, Bedoui S, et al. Migratory dendritic cells transfer antigen to a lymph noderesident dendritic cell population for efficient CTL priming. Immunity. 2006;25(1):153-162. (Pubitemid 44066832)
28. Belz GT, Shortman K, Bevan MJ, Heath WR. CD8alpha+ dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J Immunol. 2005;175(1):196-200. (Pubitemid 40884318)
29. Mueller SN, Jones CM, Smith CM, Heath WR, Carbone FR. Rapid cytotoxic T lymphocyte activation occurs in the draining lymph nodes after cutaneous herpes simplex virus infection as a result of early antigen presentation and not the presence of virus. J Exp Med. 2002;195(5):651-656. (Pubitemid 34461510)
30. Mintern J, Li M, Davey GM, et al. The use of carboxyfluorescein diacetate succinimidyl ester to determine the site, duration and cell type responsible for antigen presentation in vivo. Immunol Cell Biol. 1999;77(6):539-543.
31. Anderson BE, McNiff J, Yan J, et al. Memory CD4+ T cells do not induce graft-versus-host disease. J Clin Invest. 2003;112(1):101-108. (Pubitemid 38056381)
32. Barnden MJ, Allison J, Heath WR, Carbone FR. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and betachain genes under the control of heterologous regulatory elements. Immunol Cell Biol. 1998;76(1):34-40. (Pubitemid 28194695)
33. Kenna TJ, Waldie T, McNally A, et al. Targeting antigen to diverse APCs inactivates memory CD8+ T cells without eliciting tissue-destructive effector function. J Immunol. 2010;184(2):598-606.
34. Doan T, McNally A, Thomas R, Steptoe RJ. Steady-state dendritic cells continuously inactivate T cells that escape thymic negative selection. Immunol Cell Biol. 2009;87(8):615-622.
35. Scott CL, Robb L, Papaevangeliou B, Mansfield R, Nicola NA, Begley CG. Reassessment of interactions between hematopoietic receptors using common beta-chain and interleukin-3-specific receptor beta-chain-null cells: no evidence of functional interactions with receptors for erythropoietin, granulocyte colony-stimulating factor, or stem cell factor. Blood. 2000;96(4):1588-1590. (Pubitemid 30658496)
36. Jasperson LK, Bucher C, Panoskaltsis-Mortari A, et al. Indoleamine 2,3-dioxygenase is a critical regulator of acute graft-versus-host disease lethality. Blood. 2008;111(6):3257-3265.
37. Jung S, Unutmaz D, Wong P, et al. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity. 2002;17(2):211-220. (Pubitemid 35245963)
38. Summers-DeLuca LE, McCarthy DD, Cosovic B, et al. Expression of lymphotoxin-alphabeta on antigen-specific T cells is required for DC function. J Exp Med. 2007;204(5):1071-1081. (Pubitemid 46798151)
39. Elie R, Lapp WS. Graft-versus-host induced immunosuppression: depressed T cell helper function in vitro. Cell Immunol. 1976;21(1):31-39.
40. Hurtenbach U, Tsuchida T, Shearer GM. Modulation of T cell differentiation, antigen expression, and radiosensitivity of suppressor cells during late phases of graft-versus-host reactivity. Transplantation. 1984;38(3):256-262. (Pubitemid 14035175)
41. Waskow C, Liu K, Darrasse-Jeze G, et al. The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat Immunol. 2008;9(6):676-683. (Pubitemid 351712638)
42. Liu K, Nussenzweig MC. Origin and development of dendritic cells. Immunol Rev. 2010;234(1):45-54.
43. Bogunovic M, Ginhoux F, Helft J, et al. Origin of the lamina propria dendritic cell network. Immunity. 2009;31(3):513-525.
44. Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity. 2003;19(1):59-70. (Pubitemid 36859901)
45. Nagai Y, Garrett KP, Ohta S, et al. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity. 2006;24(6):801-812. (Pubitemid 43867369)
46. Burgdorf S, Kautz A, Bohnert V, Knolle PA, Kurts C. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science. 2007;316(5824):612-616. (Pubitemid 46683149)
47. Hill GR, Tey SK, Beagley L, et al. Successful immunotherapy of HCMV disease using virus-specific T cells expanded from an allogeneic stem cell transplant recipient. Am J Transplant. 2010; 10(1):173-179.
48. Di Stasi A, Tey SK, Dotti G, et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N Engl J Med. 2011;365(18):1673-1683.
49. Mittag D, Proietto AI, Loudovaris T, et al. Human dendritic cell subsets from spleen and blood are similar in phenotype and function but modified by donor health status. J Immunol. 2011;186(11):6207-6217.
50. Daro E, Pulendran B, Brasel K, et al. Polyethylene glycol-modified GM-CSF expands CD11b(high)- CD11c(high) but not CD11b(low)CD11c(high) murine dendritic cells in vivo: a comparative analysis with Flt3 ligand. J Immunol. 2000;165(1):49-58. (Pubitemid 30429489)